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Water, Air, & Soil Pollution

, 229:44 | Cite as

Effects of Glyphosate on Somatic and Ovarian Growth in the Estuarine Crab Neohelice granulata, During the Pre-Reproductive Period

  • Luciana Avigliano
  • Ivana S. Canosa
  • Daniel A. Medesani
  • Enrique M. Rodríguez
Article

Abstract

Adult females of the estuarine crab Neohelice granulata were exposed during the 3-month pre-reproductive period (winter) to the herbicide glyphosate, the most used pesticide in Argentina, at three different concentrations (0.02, 0.2, and 1 mg/L, as active ingredient). At the end of the in vivo assay, the body weight gain and the ovarian growth were estimated, the last one in terms of the gonadosomatic index (GSI), the relative proportion of the different kind of oocytes, and their relative size. A decrease in the body weight gain was observed by effect of pure glyphosate, at all concentrations assayed. Although no differences in either the GSI or vitellogenic protein content of the ovary were noted between any glyphosate concentration and control, a higher proportion of reabsorbed vitellogenic oocytes was observed in the ovaries of crabs exposed to glyphosate at 1 mg/L, together with an increased area of previtellogenic oocytes. These effects were confirmed in vitro, at a glyphosate concentration of 0.2 mg/L. In fact, a higher area of previtellogenic oocytes was seen when glyphosate was added to the culture medium containing ovarian tissue, but a significant higher incidence of reabsorbed vitellogenic oocytes was seen only when eyestalk tissue was also added to the vials, suggesting that the secretion of some neurohormone involved in reabsorption is enhanced. The obtained results indicate that glyphosate is able to harm, in the studied species, both somatic and the ovarian growth.

Keywords

Estuarine crabs Glyphosate Reproduction Ovarian growth Oocytes 

Notes

Acknowledgements

This study was supported by grants from both CONICET (PIP2015, code 11220150100100CO) and the University of Buenos Aires (UBACYT 2016 scientific program, code 20020150100060BA).

References

  1. American Public Health Association, American Water Works Association, & Water Pollution Control Federation. (2005). Standard methods for the examination of water and wastewaters (21th ed.). Washington, DC: American Public Health Association.Google Scholar
  2. Arancibia, F. (2013). Challenging the bioeconomy: The dynamics of collective action in Argentina. Technology in Society, 35, 79–22.CrossRefGoogle Scholar
  3. Avigliano, L., Álvarez, N. B., Mac Loughlin, C., & Rodríguez, E. M. (2014a). Effects of glyphosate on egg incubation, larvae hatching and ovarian re-maturation, in the estuarine crab Neohelice granulata. Environmental Toxicology and Chemistry, 33, 1879–1884.CrossRefGoogle Scholar
  4. Avigliano, L., Fassiano, A. V., Medesani, D. A., Ríos de Molina, M. R., & Rodríguez, E. M. (2014b). Effects of glyphosate on growth rate, metabolic rate and energy reserves of early juvenile crayfish, Cherax quadricarinatus. Bulletin of Environmental Contamination and Toxicology, 92, 631–635.CrossRefGoogle Scholar
  5. Brodeur, J. C., Suarez, R. P., Natale, G. S., Ronco, A. E., & Zaccagnini, M. E. (2011). Reduced body condition and enzymatic alterations in frogs inhabiting intensive crop production areas. Ecotoxicology and Environmental Safety, 74, 1370–1380.CrossRefGoogle Scholar
  6. Carlisle, S. M., & Trevors, J. T. (1988). Glyphosate in the environment. Water, Air, and Soil Pollution, 39, 409–420.Google Scholar
  7. Chang, E. S., Chang, S. A., Keller, R., Reddy, P. S., Snyder, M. J., & Spees, J. L. (1999). Quantification of stress in lobsters: Crustacean hyperglycemic hormone, stress protein and gene expression. American Zoologist, 39, 487–495.CrossRefGoogle Scholar
  8. Charmantier, G., Charmantier Daures, M., & Van Herp, F. (1997). Hormonal regulation of growth and reproduction in crustaceans. In M. Fingerman, R. Nagabhushanam, & M. F. Thompson (Eds.), Recent advances in marine biotechnology (Vol. I, pp. 109–161). New Delhi: Oxford and IBH Publishing.Google Scholar
  9. Chaulet, A., Medesani, D. A., Freitas, J., Cervino, A., Cervino, N., & Rodríguez, E. M. (2012). Induction of somatic growth in juvenile crayfish Cherax quadricarinatus (Decapoda, Parastacidae), by ecdysone and insulin growth factor. Aquaculture, 370–371, 1–6.CrossRefGoogle Scholar
  10. Comisión Administradora del Río de la Plata. (1990). Estudio para la evaluación de la contaminación en el Río de la Plata. Buenos Aires: Argentine Hydrographic Service Navy.Google Scholar
  11. Cooke, I. M., Haylett, B. A., & Weatherby, T. M. (1977). Electrically elicited neurosecretory and electrical responses of the isolated crab sinus gland in normal and reduced calcium salines. The Journal of Experimental Biology, 101, 125–149.Google Scholar
  12. De Kleijn, D. P. V., & Van Herp, F. (1998). Involvement of the hyperglycemic neurohormone family in the control of reproduction in decapod crustaceans. Invertebrate Reproduction and Development, 33, 263–272.CrossRefGoogle Scholar
  13. Dreon, M. S., Heras, H., & Pollero, R. J. (2003). Metabolism of ovorubin, the major egg lipoprotein from the apple snail. Molecular and Cellular Biochemistry, 243, 9–14.CrossRefGoogle Scholar
  14. Fanjul-Moles, M. L. (2006). Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: Review and update. Comparative Biochemistry and Physiology, 142C, 390–400.Google Scholar
  15. Frontera, J. L., Vatnick, I., Chaulet, A., & Rodríguez, E. M. (2011). Effects of glyphosate and polyoxyethylenamine on growth and energetic reserves in the freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Archives of Environmental Contamination and Toxicology, 61, 590–598.CrossRefGoogle Scholar
  16. García, F., Cunningham, M. L., Garda, H., & Heras, H. (2008). Embryo lipoproteins and yolk lipovitellin consumption during embryogenesis in Macrobrachium borellii (Crustacea: Palaemonidae). Journal of Comparative Physiology, 151B, 317–322.Google Scholar
  17. Hyne, R. V. (2011). Review of the reproductive biology of amphipods and their endocrine regulation: Identification of mechanistic pathways for reproductive toxicants. Environmental Toxicology and Chemistry, 30, 2647–2657.CrossRefGoogle Scholar
  18. LeBlanc, G. A. (2007). Crustacean endocrine toxicology: A review. Ecotoxicology, 16, 61–81.CrossRefGoogle Scholar
  19. Leguizamón, A. (2014). Modifying Argentina: GM soy and socio-environmental change. Geoforum, 53, 149–160.CrossRefGoogle Scholar
  20. López Greco, L. S., & Rodríguez, E. M. (1999). Annual reproduction and growth of adult crabs, Chasmagnathus granulata (Crustacea, Brachyura, Grapsidae). Cahiers de Biologie Marine, 40, 155–164.Google Scholar
  21. Lydon, J., & Duke, S. O. (1989). Pesticide effects on secondary metabolism of greater plants. Pesticide Science, 25, 361–373.CrossRefGoogle Scholar
  22. Mensah, P. K., Muller, W. J., & Palmer, C. G. (2012). Using growth measures in the freshwater shrimp Caridina nilotica as biomarkers of roundup® pollution of south African freshwater systems. Physics and Chemistry of the Earth, 50–52, 262–268.CrossRefGoogle Scholar
  23. Mesnage, R., Defarge, N., Spiroux de Vendômois, J., & Séralini, G. E. S. (2015). Potential toxic effects of glyphosate and its commercial formulations below regulatory limits. Food and Chemical Toxicology, 84, 133–153.CrossRefGoogle Scholar
  24. Nagaraju, G. P. C. (2011). Reproductive regulators in decapod crustaceans: An overview. The Journal of Experimental Biology, 214, 3–16.CrossRefGoogle Scholar
  25. Peruzzo, P. J., Porta, A. A., & Ronco, A. E. (2008). Levels of glyphosate in surface waters, sediments and soil associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environmental Pollution, 156, 61–66.CrossRefGoogle Scholar
  26. Quassinti, L., Maccari, E., Murri, O., & Bramucci, M. (2009). Effects of paraquat and glyphosate on steroidogenesis in gonads of the frog Rana esculenta in vitro. Pesticide Biochemistry and Physiology, 93, 91–95.CrossRefGoogle Scholar
  27. Richard, S., Moslemi, S., Sipahutar, H., Benachour, N., & Seralini, G. E. (2005). Differential effects of glyphosate and roundup on human placental cells and aromatase. Environmental Health Perspectives, 113, 716–720.CrossRefGoogle Scholar
  28. Rodríguez, E. M., & Pisanó, A. (1993). Effects of parathion and 2-4 D to egg incubation and larvae hatching in Chasmagnathus granulata (Decapoda, Brachyura). Comparative Biochemistry and Physiology, 104C, 71–78.Google Scholar
  29. Rodríguez, E. M., Schuldt, M., & Romano, L. (1994). Chronic histopathological effects of parathion and 2,4-D on female gonads of Chasmagnathus granulata (Decapoda, Brachyura). Food and Chemical Toxicology, 32, 811–818.CrossRefGoogle Scholar
  30. Rodríguez, E. M., López Greco, L. S., & Fingerman, M. (2000). Inhibition of ovarian growth by cadmium, in the fiddler crab Uca pugilator (Decapoda, Ocypodidae). Ecotoxicology and Environmental Safety, 46, 202–206.CrossRefGoogle Scholar
  31. Rodríguez, E. M., Medesani, D. A., & Fingerman, M. (2007). Endocrine disruption in crustaceans due to pollutants: A review. Comparative Biochemistry and Physiology, 146A, 661–671.CrossRefGoogle Scholar
  32. Roy, N. M., Carneiro, B., & Ochs, J. (2016). Glyphosate induces neurotoxicity in zebrafish. Environmental Toxicology and Pharmacology, 42, 45–54.CrossRefGoogle Scholar
  33. Sánchez, M. V., Cahansky, A. V., López Greco, L. S., & Rodríguez, E. M. (2005). Toxicity of mercury during the embryonic development of Chasmagnathus granulatus (Brachyura, Varunidae). Environmental Research, 99, 72–78.CrossRefGoogle Scholar
  34. Sarojini, R., Nagabhushanam, R., & Fingerman, M. (1997). An in vitro study of the inhibitory action of methionine enkephaline on ovarian maturation in the red swamp crayfish, Procambarus clarkii. Comparative Biochemistry and Physiology, 117C, 207–210.Google Scholar
  35. Sokal, R. R., & Rohlf, F. J. (1981). Biometry (2nd ed.). New York: Freeman.Google Scholar
  36. Sokolova, I. M., Frederich, M., Bagwe, R., Lannig, G., & Sukhotin, A. A. (2012). Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance n aquatic invertebrates. Marine Environmental Research, 79, 1–15.CrossRefGoogle Scholar
  37. Zapata, V., López Greco, L. S., & Rodríguez, E. M. (2001). Effect of copper on hatching and development of larvae of the estuarine crab Chasmagnathus granulata (Decapoda, Brachyura). Environmental Toxicology and Chemistry, 20, 1579–1583.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Dept. of Biodiversity and Experimental Biology, FCENUniversity of Buenos Aires. Institute of Biodiversity, Experimental and Applied Biology (IBBEA), CONICET-UBA. Ciudad UniversitariaBuenos AiresArgentina

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